Abstract
1. In Lymnaea stagnalis L. (Pulmonata, Basommatophora) the neurons in the osphradium were visualized by staining through the inner right parietal nerve by 5,6-carboxyfluorescein (5,6-CF). Three types of neurons were identified: three large ganglionic cells (GC1-3; 80–100 μm), the small putative sensory neurons (SC; 20 μm) and very small sensory cells (3–5 μm).
2. The ganglionic and putative sensory neurons were investigated by whole cell patch-clamp method in current-clamp condition. The three giant ganglionic neurons (GC1-3) located closely to the root of osphradial nerve, had a membrane potential (MP) between −30 and −70 mV and showed tonic or bursting activities. The small putative sensory cells (SCs) scattered throughout the osphradial ganglion, possessed a MP between −25 and −55 mV and showed an irregular firing pattern with membrane oscillations. At resting MP the GC1-3 cells were depolarized and increased the frequency of their firing, while the SCs were hyperpolarized and inhibited by NaCl (10−2 M) and L-aspartate (10−5 M) applied to the osphradium.
3. 5-Hydroxytryptamine (5HT, 10−6 M), γ-aminobutyric acid (GABA; 10−6 M) and the GABAB agonist baclofen (10−6 M) depolarized the neurons GC1-3 and increased their firing frequency. In contrast, on the GC1-3 neurons, acetylcholine (Ach; 10−6 M) and FMRFamide (10−6 M) caused hyperpolarization and cessation of the firing activity. The 5HT effect was blocked by mianserin (10−6 M) but picrotoxin (10−5 M) failed to block the GABA-induced effect on the GC1-3 cells.
4. The small putative sensory neurons (SCs) were excited by Ach (10−6 M) and 5HT (10−6 M) but were inhibited by GABA (10−6 M). FMRFamide (10−6 M) had a biphasic response. The Ach effect was blocked by hexamethonium (10−6 M) and tetraethylammonium (10−6 M), indicating the involvement of nicotinic cholinergic receptors.
5. The distinct responses of the two populations of osphradial neurons to chemical stimuli and neurotransmitters suggest that they can differently perceive signals from environment and hemolymph.
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REFERENCES
Bailey, D. F., and Benjamin, P. R. (1968). Anatomical and electrophysiological studies on the gastropod osphradium. Symp. Zool. Soc. Lond. 23:263–268.
Benjamin, P. R. (1971). On the structure of the pulmonate osphradium. I. Cell types and their organization. Z. Zellforsch. Mikrosk. Anat. 117:485–501.
Benjamin, P. R., and Peat, A. (1971). On the structure of the pulmonate osphradium. II. Ultrastructure. Z. Zellforsch. Mikrosk. Anat. 118:168–189.
Croll, R. P. (1983). Gastropod chemoreception. Biol. Rev. 58:293–319.
De Wilt, G., van der Roest, M., and Janse C. (1988). The role of the two peptidergic giant neurons in modulations of respiratory behaviour in the pond snail, Lymnaea stagnalis. In Salánki, J., and S.-Rózsa, K. (eds.), Neurobiology of Invertebrates, Symp. Biol. Hung. Vol. 36, Akadémiai Kiadó, Budapest, pp. 377–386.
De Wilt, G., Li, K. W., van Minnen, J., van der Schors, R. C., Smit, A. B., Thijsen, S.F. T., and Boer, H. H. (1991). Neuroendocrine control of hydromineral regulation in the freshwater snail Lymnaea stagnalis. In Kits, K. S., Boer, H. H., and Joosse, J. (eds.), Molluscan Neurobiology, North-Holland, Amsterdam/Oxford/New York, pp. 335–339.
Hamill, O. P., Marty, A., Neher, E., Sakmann, B., and Sigworth, F. J. (1981). Improved patch-clamp techniques for high resolution current recording from cells and cell-free membrane patches. Pflügers Arch. 391:85–100.
Haszprunar, G. (1987). The fine morphology of the osphradial sense organs of the Mollusca. I. Gastropoda, Prosobranchia. Phil. Trans. R. Soc. Lond. B 307:457–496.
Jahan-Parwar, B. (1972). Behavioral and electrophysiological studies on chemoreception of Aplysia. Am Zool. 12:525–537.
Janse, C., van der Wilt, G., van der Plas, J., and van der Roest, M. (1985). Central and peripheral neurons involved in oxygen perception in the pulmonate snail, Lymnaea stagnalis (Mollusca, Gastropoda). Comp. Biochem. Physiol. 4:1–29.
Janse, C., van der Wilt, G., van der Roest, M., and Pieneman, A. W. (1988). Modulation of primary sensory neurons and its relevance to behavior in the pond snail, Lymnaea stagnalis. In Salánki, J. and S.-Rózsa, K. (eds.), Neurobiology of Invertebrates. Transmitters, Modulators and Receptors, Akadémiai Kiadó, Budapest, pp. 559–568.
Kamardin, N. N. (1976). The structure and cellular organization of the osphradium in Lymnaea stagnalis. Arch. Anat. Histol. Embriol. 71:87–90 (in Russian).
Kamardin, N. N. (1995). The electrical responses of osphradial nerve and central neurons to chemical stimulation of Lymnaea osphradium. In Salánki, J., S.-Rózsa, K., and Elekes, K. (eds.), Neurobiology of Invertebrates. Simple and Complex Regulatory Systems, Akadémiai Kiadó, Budapest, pp. 315–320.
Kamardin, N. N., and Tsirulis, T. P. (1980). Electron-microscopy study of Lymnaea osphradium. Tsitologia 22:266–270 (in Russian).
Kemenes, G., and Elliot, C. J. H. (1994). Analysis of the feeding motor pattern in the pond snail, Lymnaea stagnalis: Photoinactivation of axonally stained pattern generating interneurons. J. Neurosci. 14:153–166.
Kemenes, G., Daykin, K., and Elliot, C. J. H. (1991). Photoinactivation of neurons axonally filled with the fluorescent dye 5(6) carboxyfluorescein in the pond snail, Lymnaea stagnalis. J. Neurosci. Meth. 39:207–216.
Kits, K. S. (1980). States of excitability in ovulation hormone producing neuroendocrine cells of Lymnaea stagnalis (Gastropoda) and their relation to the egg-laying cycle. J. Neurobiol. 11:397–410.
Nezlin, L. P. (1995). Primary sensory neurons and their central projections in the pond snail Lymnaea stagnalis. In Salánki, J., S.-Rózsa, K., and Elekes, K. (eds.), Neurobiology of Invertebrates. Simple and Complex Regulatory Systems, Akadémiai Kiadó, Budapest, pp. 305–313.
Nezlin, L. P., Moroz, L. L., Elofsson, R., and Sakharov, D. A. (1994). Immunolabelled neuroactive substances in the osphradium of the pond snail, Lymnaea stagnalis. Cell Tissue Res. 275:269–275.
Ridgway, R. L., and Bulloch A. G. M. (1991). Glutamate modulation of sprouting by adult Helisoma neurons. In Kits, K. S., Boer, H. H., and Joosse, J. (eds.), Molluscan Neurobiology, North-Holland, Amsterdam/Oxford/New York, pp. 154–160.
Salánki, J., and S.-Rózsa, K. (1986). Interaction of opioid peptides and low-molecular-weight neurotransmitters in Helix neurons. In Stefano, G. B. (ed.), Handbook of Comparative Opioid and Related Neuropeptide Mechanisms, Vol. II, CRC Press, Boca Raton, FL. pp. 103–113.
S.-Rózsa, K. (1979). Analysis of the neural network regulating the cardio-renal system in the central nervous system of Helix pomatia L. Am. Zool. 19:117–128.
S.-Rózsa, K. (1995). Two types of reorganization in multifunctional neural networks of Helix pomatia L. Acta Biol. Hung. 46:247–262.
S.-Rózsa, K., and Dyakonova (1989). Interaction of serotonin and leu-enkephalin on the habituating central neurons of Helix pomatia L. in situ and in vitro. Comp. Biochem. Physiol. C 92:361–370.
S.-Rózsa, K., and Solntseva, E. V. (1986). Modulation of cholinergic transmission by opioid peptides and FMRFamide on identified neurons of Helix pomatia L. (Gastropoda, Mollusca). Acta Physiol. Hung. 67:429–433.
S.-Rózsa, K., et al. (1996). Met-enkephalin and morphiceptin modulate a GABA-induced inward current in the CNS of Lymnaea stagnalis L. Gen Pharmacol. 27:1337–1345.
Sokolov, V. A., Kamardin, N. N., Zaitseva, O. V., and Tsirulis, T. P. (1980). Osphradial sensory system of gastropod molluscs. In Sokolov, V. A. (ed.), Sensory Systems, Nauka, Leningrad, pp. 159–176 (in Russian).
Stinnakre, J., and Tauc, L. (1969). Central neuronal response to the activation of the osmoreceptors in the osphradium of Aplysia. J. Exp. Biol. 51:347–361.
Wedemeyer, H., and Schild, D. (1995). Chemosensitivity of the osphradium of the pond snail Lymnaea stagnalis. J. Exp. Biol. 198:1743–1754.
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Kamardin, N., Szűcs, A. & -Rózsa, K. Distinct Responses of Osphradial Neurons to Chemical Stimuli and Neurotransmitters in Lymnaea stagnalis L.. Cell Mol Neurobiol 19, 235–247 (1999). https://doi.org/10.1023/A:1006929211493
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DOI: https://doi.org/10.1023/A:1006929211493